Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i>
We previously reported that proline modulates root meristem size in <i>Arabidopsis</i> by controlling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O<sub>2</sub><sup>•−</sup>...
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MDPI AG
2022-06-01
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| Series: | Plants |
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| Online Access: | https://www.mdpi.com/2223-7747/11/11/1512 |
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| author | Sara Bauduin Martina Latini Irene Belleggia Marta Migliore Marco Biancucci Roberto Mattioli Antonio Francioso Luciana Mosca Dietmar Funck Maurizio Trovato |
| author_facet | Sara Bauduin Martina Latini Irene Belleggia Marta Migliore Marco Biancucci Roberto Mattioli Antonio Francioso Luciana Mosca Dietmar Funck Maurizio Trovato |
| author_sort | Sara Bauduin |
| collection | DOAJ |
| description | We previously reported that proline modulates root meristem size in <i>Arabidopsis</i> by controlling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O<sub>2</sub><sup>•−</sup>) and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), which, in turn, modulate root meristem size and root elongation. We found that hydrogen peroxide plays a major role in proline-mediated root elongation, and its effects largely overlap those induced by proline, influencing root meristem size, root elongation, and cell cycle. Though a combination of genetic and pharmacological evidence, we showed that the short-root phenotype of the proline-deficient <i>p5cs1 p5cs2/P5CS2</i>, an <i>Arabidopsis</i> mutant homozygous for <i>p5cs1</i> and heterozygous for <i>p5cs2</i>, is caused by H<sub>2</sub>O<sub>2</sub> accumulation and is fully rescued by an effective H<sub>2</sub>O<sub>2</sub> scavenger. Furthermore, by studying <i>Arabidopsis</i> mutants devoid of ProDH activity, we disclosed the essential role of this enzyme in the modulation of root meristem size as the main enzyme responsible for H<sub>2</sub>O<sub>2</sub> production during proline degradation. Proline itself, on the contrary, may not be able to directly control the levels of H<sub>2</sub>O<sub>2</sub>, although it seems able to enhance the enzymatic activity of catalase (CAT) and ascorbate peroxidase (APX), the two most effective scavengers of H<sub>2</sub>O<sub>2</sub> in plant cells. We propose a model in which proline metabolism participates in a delicate antioxidant network to balance H<sub>2</sub>O<sub>2</sub> formation and degradation and fine-tune root meristem size in <i>Arabidopsis</i>. |
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| institution | Directory Open Access Journal |
| issn | 2223-7747 |
| language | English |
| last_indexed | 2024-03-10T00:57:57Z |
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| spelling | doaj.art-9fad6341a3264f4b81ceadf4cfb9155c2023-11-23T14:39:52ZengMDPI AGPlants2223-77472022-06-011111151210.3390/plants11111512Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i>Sara Bauduin0Martina Latini1Irene Belleggia2Marta Migliore3Marco Biancucci4Roberto Mattioli5Antonio Francioso6Luciana Mosca7Dietmar Funck8Maurizio Trovato9Department of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biochemical Sciences, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biochemical Sciences, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Biology, University of Konstanz, 78457 Konstanz, GermanyDepartment of Biology and Biotechnology, Sapienza University of Rome, 00185 Rome, ItalyWe previously reported that proline modulates root meristem size in <i>Arabidopsis</i> by controlling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O<sub>2</sub><sup>•−</sup>) and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), which, in turn, modulate root meristem size and root elongation. We found that hydrogen peroxide plays a major role in proline-mediated root elongation, and its effects largely overlap those induced by proline, influencing root meristem size, root elongation, and cell cycle. Though a combination of genetic and pharmacological evidence, we showed that the short-root phenotype of the proline-deficient <i>p5cs1 p5cs2/P5CS2</i>, an <i>Arabidopsis</i> mutant homozygous for <i>p5cs1</i> and heterozygous for <i>p5cs2</i>, is caused by H<sub>2</sub>O<sub>2</sub> accumulation and is fully rescued by an effective H<sub>2</sub>O<sub>2</sub> scavenger. Furthermore, by studying <i>Arabidopsis</i> mutants devoid of ProDH activity, we disclosed the essential role of this enzyme in the modulation of root meristem size as the main enzyme responsible for H<sub>2</sub>O<sub>2</sub> production during proline degradation. Proline itself, on the contrary, may not be able to directly control the levels of H<sub>2</sub>O<sub>2</sub>, although it seems able to enhance the enzymatic activity of catalase (CAT) and ascorbate peroxidase (APX), the two most effective scavengers of H<sub>2</sub>O<sub>2</sub> in plant cells. We propose a model in which proline metabolism participates in a delicate antioxidant network to balance H<sub>2</sub>O<sub>2</sub> formation and degradation and fine-tune root meristem size in <i>Arabidopsis</i>.https://www.mdpi.com/2223-7747/11/11/1512antioxidant enzymes<i>Arabidopsis</i>hydrogen peroxide<i>prodh1 prodh2</i><i>p5cs1 p5cs2/P5CS2</i>proline |
| spellingShingle | Sara Bauduin Martina Latini Irene Belleggia Marta Migliore Marco Biancucci Roberto Mattioli Antonio Francioso Luciana Mosca Dietmar Funck Maurizio Trovato Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> Plants antioxidant enzymes <i>Arabidopsis</i> hydrogen peroxide <i>prodh1 prodh2</i> <i>p5cs1 p5cs2/P5CS2</i> proline |
| title | Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> |
| title_full | Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> |
| title_fullStr | Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> |
| title_full_unstemmed | Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> |
| title_short | Interplay between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in <i>Arabidopsis</i> |
| title_sort | interplay between proline metabolism and ros in the fine tuning of root meristem size in i arabidopsis i |
| topic | antioxidant enzymes <i>Arabidopsis</i> hydrogen peroxide <i>prodh1 prodh2</i> <i>p5cs1 p5cs2/P5CS2</i> proline |
| url | https://www.mdpi.com/2223-7747/11/11/1512 |
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